The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX
Pseudomonas aeruginosa is a highly adaptable Gram-negative opportunistic pathogen, notably due to its large number of transcription regulators. The extracytoplasmic sigma factor (ECFσ) AlgU, responsible for alginate biosynthesis, is also involved in responses to cell wall stress and heat shock via t...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-10-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2020.579495/full |
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| author | Emeline Bouffartigues Ishac Si Hadj Mohand Olivier Maillot Damien Tortuel Jordane Omnes Audrey David Ali Tahrioui Rachel Duchesne Cecil Onyedikachi Azuama Michael Nusser Gerald Brenner-Weiss Alexis Bazire Nathalie Connil Nicole Orange Marc G. J. Feuilloley Olivier Lesouhaitier Alain Dufour Pierre Cornelis Sylvie Chevalier |
| author_facet | Emeline Bouffartigues Ishac Si Hadj Mohand Olivier Maillot Damien Tortuel Jordane Omnes Audrey David Ali Tahrioui Rachel Duchesne Cecil Onyedikachi Azuama Michael Nusser Gerald Brenner-Weiss Alexis Bazire Nathalie Connil Nicole Orange Marc G. J. Feuilloley Olivier Lesouhaitier Alain Dufour Pierre Cornelis Sylvie Chevalier |
| author_sort | Emeline Bouffartigues |
| collection | DOAJ |
| description | Pseudomonas aeruginosa is a highly adaptable Gram-negative opportunistic pathogen, notably due to its large number of transcription regulators. The extracytoplasmic sigma factor (ECFσ) AlgU, responsible for alginate biosynthesis, is also involved in responses to cell wall stress and heat shock via the RpoH alternative σ factor. The SigX ECFσ emerged as a major regulator involved in the envelope stress response via membrane remodeling, virulence and biofilm formation. However, their functional interactions to coordinate the envelope homeostasis in response to environmental variations remain to be determined. The regulation of the putative cmaX-cfrX-cmpX operon located directly upstream sigX was investigated by applying sudden temperature shifts from 37°C. We identified a SigX- and an AlgU- dependent promoter region upstream of cfrX and cmaX, respectively. We show that cmaX expression is increased upon heat shock through an AlgU-dependent but RpoH independent mechanism. In addition, the ECFσ SigX is activated in response to valinomycin, an agent altering the membrane structure, and up-regulates cfrX-cmpX transcription in response to cold shock. Altogether, these data provide new insights into the regulation exerted by SigX and networks that are involved in maintaining envelope homeostasis. |
| first_indexed | 2024-12-12T22:54:18Z |
| format | Article |
| id | doaj.art-30af852463fe40219f453eb952ec5966 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-12T22:54:18Z |
| publishDate | 2020-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-30af852463fe40219f453eb952ec59662022-12-22T00:08:59ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-10-011110.3389/fmicb.2020.579495579495The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigXEmeline Bouffartigues0Ishac Si Hadj Mohand1Olivier Maillot2Damien Tortuel3Jordane Omnes4Audrey David5Ali Tahrioui6Rachel Duchesne7Cecil Onyedikachi Azuama8Michael Nusser9Gerald Brenner-Weiss10Alexis Bazire11Nathalie Connil12Nicole Orange13Marc G. J. Feuilloley14Olivier Lesouhaitier15Alain Dufour16Pierre Cornelis17Sylvie Chevalier18Laboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceInstitute of Functional Interfaces, Karlsruhe Institute of Technology, Karlsruhe, GermanyInstitute of Functional Interfaces, Karlsruhe Institute of Technology, Karlsruhe, GermanyLaboratoire de Biotechnologie et Chimie Marines (LBCM) EA3884, IUEM, Université de Bretagne-Sud, Lorient, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Biotechnologie et Chimie Marines (LBCM) EA3884, IUEM, Université de Bretagne-Sud, Lorient, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FranceLaboratoire de Microbiologie Signaux et Microenvironnement (LMSM) EA 4312, Normandie Université, Université de Rouen Normandie, Centre de Sécurité Sanitaire de Normandie, Evreux, FrancePseudomonas aeruginosa is a highly adaptable Gram-negative opportunistic pathogen, notably due to its large number of transcription regulators. The extracytoplasmic sigma factor (ECFσ) AlgU, responsible for alginate biosynthesis, is also involved in responses to cell wall stress and heat shock via the RpoH alternative σ factor. The SigX ECFσ emerged as a major regulator involved in the envelope stress response via membrane remodeling, virulence and biofilm formation. However, their functional interactions to coordinate the envelope homeostasis in response to environmental variations remain to be determined. The regulation of the putative cmaX-cfrX-cmpX operon located directly upstream sigX was investigated by applying sudden temperature shifts from 37°C. We identified a SigX- and an AlgU- dependent promoter region upstream of cfrX and cmaX, respectively. We show that cmaX expression is increased upon heat shock through an AlgU-dependent but RpoH independent mechanism. In addition, the ECFσ SigX is activated in response to valinomycin, an agent altering the membrane structure, and up-regulates cfrX-cmpX transcription in response to cold shock. Altogether, these data provide new insights into the regulation exerted by SigX and networks that are involved in maintaining envelope homeostasis.https://www.frontiersin.org/articles/10.3389/fmicb.2020.579495/fullPseudomonas aeruginosatemperaturecell wall stress ECF sigma factorregulation of transcriptionmembrane fluidity |
| spellingShingle | Emeline Bouffartigues Ishac Si Hadj Mohand Olivier Maillot Damien Tortuel Jordane Omnes Audrey David Ali Tahrioui Rachel Duchesne Cecil Onyedikachi Azuama Michael Nusser Gerald Brenner-Weiss Alexis Bazire Nathalie Connil Nicole Orange Marc G. J. Feuilloley Olivier Lesouhaitier Alain Dufour Pierre Cornelis Sylvie Chevalier The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX Frontiers in Microbiology Pseudomonas aeruginosa temperature cell wall stress ECF sigma factor regulation of transcription membrane fluidity |
| title | The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX |
| title_full | The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX |
| title_fullStr | The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX |
| title_full_unstemmed | The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX |
| title_short | The Temperature-Regulation of Pseudomonas aeruginosa cmaX-cfrX-cmpX Operon Reveals an Intriguing Molecular Network Involving the Sigma Factors AlgU and SigX |
| title_sort | temperature regulation of pseudomonas aeruginosa cmax cfrx cmpx operon reveals an intriguing molecular network involving the sigma factors algu and sigx |
| topic | Pseudomonas aeruginosa temperature cell wall stress ECF sigma factor regulation of transcription membrane fluidity |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2020.579495/full |
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